Diagnostic and Interventional Imaging (2015) 96, 547—562

REVIEW / Gastrointestinal imaging

Radioembolization with yttrium-90microspheres work up: Practical approachand literature review

G. Vesselle ∗, I. Petit, S. Boucebci, T. Rocher,S. Velasco, J.-P. Tasu

Functional and Therapeutic Diagnostic Imaging Unit, Poitiers University Hospital, rue de laMilétrie, 86000 Poitiers, France

KEYWORDSRadioembolization;Hepatocellularcarcinoma;Interventionaloncology;Selective internalradiotherapy;Yttrium-90

Abstract Radioembolization (RE) is a selective internal radiotherapy technique in whichyttrium-90 blended microspheres are infused through the hepatic arteries. It is based on thefact that primary and secondary hepatic tumors are vascularized mostly by arterial bloodflow whereas healthy hepatocytes obtain their blood supply mostly from the portal network.This enables high radiation doses to be delivered, sparing the surrounding non-malignant liverparenchyma. Most of the complications are caused by unexpected particles passing into thegastrointestinal tract through branches originating from the main hepatic arterial supply. Knowl-edge of this hepatic arterial network and of its variations and the technical considerations thisraises are required in preparation for treatment. This work describes the specific anatomicalfeatures and techniques for this anatomy through recent literature illustrated by cases from

our own experience. © 2014 Éditions francaises de rad

Abbreviations: CA, Celiac axis; SMA, Superior mesenteric artery; HA, Hartery; APDA, Anterosuperior pancreaticoduodenal arcade; MHA, Main heCystic artery; FA, Falciform ligament artery; RHA, Right hepatic artery; ahepatic artery; aRHA, Accessory right hepatic artery; SDA, Supraduodemacroaggregates; CT, Computer tomography; HCC, Hepatocellular cararterial chemombolization; CT, Computed tomography; rLHA, Replaced l

∗ Corresponding author.E-mail address: guillaumevesselle@gmail.com (G. Vesselle).

http://dx.doi.org/10.1016/j.diii.2014.03.0142211-5684/© 2014 Éditions francaises de radiologie. Published by Elsevie

iologie. Published by Elsevier Masson SAS. All rights reserved.

epatic artery; CHA, Common hepatic artery; GDA, Gastroduodenalpatic artery; RGA, Right gastric artery; LGA, Left gastric artery; CA,LHA, Left hepatic artery; PA, Phrenic artery; aLHA, Accessory left

nal artery; RE, Radioembolization; 90Y, Yttrium-90; AMA, Albumincinoma; MIP, Maximum Intensity Projection; TACE, Transcathetereft hepatic artery; rRHA, Replaced right hepatic artery.

r Masson SAS. All rights reserved.

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epatic radioembolization is a recent oncological interven-ional radiology technique reported for the first time in988 [1], and used to treat hepatocellular carcinoma andiver metastases. This technique involves administering glassr resin microspheres loaded with yttrium-90 through aatheter into the artery or arteries supplying target lesions.ttrium-90 is a beta emitter with a half-life of 64.053 hoursnd disintegrates into zirconium-90, which is stable. Theverage penetration of the irradiation is 2.5 mm, reaching aaximum of 10 mm. By coming closer to the target lesions

ery high doses can therefore be delivered, reducing theoxicity to the adjacent liver parenchyma, unlike externaladiotherapy [2]. Both the treatment itself and its successre governed by several stages:CT and MR for arterial mapping and to assess the hepaticlesions;arteriography, the purposes of which are to occlude thevarious arteries in the hepatic pedicle which run outsideof the liver in order to reduce extrahepatic diffusion ofthe microspheres as the extent of embolization variesbetween groups and depending on the substances usedfor treatment [3—6]; to occlude accessory arteries sup-plying the liver, attempting to achieve arterial supplyonly from the hepatic artery or its variants. The use ofcomputed tomography reconstruction mode, available onsome angiography tables, or cone-beam CT is, in the opin-ion of some authors, a valuable aid to this stage [3,5,7,8];technetium 99 scintigraphy, which is used to quantify thehepatopulmonary shunt and confirm that no extrahepaticuptake is present.

Because of the risk of radiation damage, these factorsay contraindicate treatment in some cases.This report describes each stage from our own experience

nd from the literature, with particular attention to the

echnical points which need to be understood. Each arterys described in succession, explaining its anatomy, how toecognize it on computed tomography and how to managet in the preoperative phase.

•

igure 1. a: MIP coronal reconstruction of an abdominal CT in the ardouble black arrow), common hepatic artery (small arrow), gastroduodrrow), left gastric artery (white arrowhead); b: hepatic arteriographastroduodenal artery (arrowhead) and cystic artery (arrow). Note the p

G. Vesselle et al.

In some cases, occlusion of some arteries is a real tech-ical challenge and we describe from our own experiencehe different technical options available, some of which arenspired from interventional neuroradiology techniques.

xtrahepatic branches of the hepaticedicle

astroduodenal artery

he common hepatic artery (CHA) divides into the mainepatic artery (MHA) and the gastroduodenal artery (GDA).he GDA runs along the posterior aspect of the first part ofhe duodenum, giving rise to the anterosuperior pancreati-oduodenal artery, next to the upper part of the pancreasnd divides into the inferior pancreaticoduodenal artery andhe gastro-epiploic artery, running to the inferior edge ofhe duodenum. There are many anatomical variants, somef which may impact on the procedure. These include therigin of a cystic artery (Fig. 1b) and right gastric or rightepatic artery (single or accessory).

This artery is always present and it can be easily identi-ed both on CT and on arteriography (Fig. 1).

Reflux of yttrium-90 (90Y) loaded spheres into the GDAarries a risk of pancreatitis (ischemic or radiation-induced)nd gastroduodenal ulceration, explaining why most authorsgree that it should be occluded [3,9—13]. The risk of refluxs increased if the GDA arises distally from the MHA (andarticularly if it arises from a trifurcation of the MHA intoight and left branches of the hepatic artery and GDA) [3,5].hen the decision is made to occlude this artery, it should

e occluded as proximally as possible as branches supplyingxtrahepatic regions commonly arise very early (Fig. 1b).ossible collateral branches should also be looked for andccluded [2,11] (Figs. 2 and 3).

Occlusion of this artery is debatable in two situations:

in the presence of retrograde flow (hepatopetic), a situ-ation usually seen in tight stenoses or obstruction of theceliac axis (CA), occluding the artery, is of no benefit andmay even be potentially harmful in this situation [14—16];

terial phase. Celiac axis (black arrow), superior mesenteric arteryenal artery (black arrowhead), main hepatic artery (double smally with opacification of the common hepatic artery, showing theresence of many gallstones.

Radioembolization with yttrium-90 microspheres work up 549

Figure 2. Occlusion of the gastroduodenal artery in a 50-year-old male patient. The gastroduodenal artery (arrowhead) and adjacentrecanhat th

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collateral artery (arrow) is seen (a). Coil occlusion and immediate

of a collateral branch (arrow) (b) requiring its occlusion (c). Note t

• if the decision is made to carry out distal selective injec-tion, the risk of reflux into the artery is then very low [2].This approach is favored by several authors who recom-mend injecting as distally as possible, fractionating thedose if necessary, and thereby avoiding occlusion of theGDA and reducing the development of collaterals [6,13].

The GDA is generally straightforward to catheterize witha microguide-assisted microcatheter.

Technical tipsThe GDA is usually occluded by coiling (hydrocoils or metalcoils) (Fig. 2c) [17]. As the packing remains mobile for as longas thrombus does not form, the risk of migration may remainwhen the artery is wide in diameter and therefore requiresa large number of coils (up to 8 in our experience). This risk

can be reduced by the anchoring technique which involvesdeploying the start of the first coil in a collateral branchand finishing deployment in the gastroduodenal artery whichacts as a support for the subsequent coils (Fig. 4).

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Figure 3. Occlusion of a branch of the gastroduodenal artery by the suartery and occlusion of the gastroduodenal artery (arrowhead). Distal

creaticoduodenal arcade supplied by a branch arising from the right bcatheterization because of the narrow diameter and stenosis in the maiperformed retrogradely through the superior mesenteric artery, enablinhepatic arterial supply originating from one of its branches (white arrow

alization distal to the packing (double arrow) by the developmente right gastric artery can be seen (white arrow).

Some authors consider that the use of a single hydro-oil of appropriate dimension can achieve occlusion andeduce costs [17] in the same way as plug occlusion [12]Fig. 5).

The angiogenesis occasionally promoted by occlusion ofhe GDA may lead to the development of potentially danger-us uncatheterizable collaterals, which raises the questionf permanent occlusion. Transient occlusion with a Hyper-orm remodeling balloon (Covidien) is another techniquehich has been recently described without complication

18].The use of microcatheters such as the Antireflux Sure-

ire Infusion System may help to avoid occlusion when it isossible to administer spheres distally to arteries supplyingxtrahepatic territories [19].

ractical considerations

cclusion of the GDA is recommended by most authors, par-icularly when it arises distal to the MHA.

It is, however, debatable or even harmful if retrogradeow is present.

perior mesenteric artery; a: arteriography of the common hepaticanastomoses seen between the gastroduodenal artery and a pan-ranch of the hepatic artery (black arrows); b: failed anterograden hepatic artery. Catheterization of the arcade (arrows) was theng it to be occluded (c). Note the cystic artery (white arrow) andhead).

550 G. Vesselle et al.

Figure 4. Opacification of the celiac axis showing the gastroduodenal artery (arrowhead) and anterosuperior pancreaticoduodenal arcade(arrow) (a). An initial coil is anchored (arrow) in the anterosuperior pancreaticoduodenal artery (b) allowing the subsequent coils to bed lete afi y (do

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eployed without migration of the packing (arrowhead) (c). Compnal control (d). Note the initial occlusion of the right gastric arter

ight gastric artery (formerly called theyloric artery)

ogether with the left gastric artery (LGA), the rightastric artery (RGA) forms the anastomotic arcade forhe lesser curvature of the stomach which they vascular-ze together with the pylorus. This is found routinely in

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igure 5. Opacification of a large gastroduodenal artery (a), plug occompletely occluded (c). Note the large arterioportal fistula (double arr

nd proximal occlusion of the gastroduodenal artery confirmed onuble arrow) (b).

ublished arteriography findings [20]. It arises usually fromhe MHA (45—57%) or the left branch of the HA (23%) andccasionally from the GDA (3—12%), the CHA (2,7—5%) or

he right branch of the HA (4%) [20,21].

It is usually identifiable on a pretreatment scan (Fig. 6).f the flow is sufficient, it can be seen on proximal arteriog-aphy by its characteristic curvature (Figs. 2c and 7).

lusion (deployment in b) followed by a check confirming that it isow).

Radioembolization with yttrium-90 microspheres work up 551

Figure 6. Axial (a) and coronal (b) MIP CT reconstructions. Left branch of the hepatic artery (arrowhead) and right gastric artery (arrow).

ing a large right gastric artery originating from the main hepatic arteryatient who had previously undergone left hepatectomy as shown by theure, extending to the left gastric artery (arrow) (b).

Figure 7. Opacification of the common hepatic artery (a) reveal(small arrows) catheterized secondarily (b) then occluded (c) in a psurgical clips (arrowhead). Note the full arcade of the lesser curvat

The complications of diffusion of microspheres into theRGA range from transient upper epigastric pain, which canbe easily relieved by standard analgesics and gastric antise-cretory agents, to antropyloric ulcers which are often largeand not well relieved by oral treatments as they are locatedin the serosa and subserosa and usually require surgery(Fig. 8) [22—24]. These different complications have beenreported frequently in the literature with a prevalence of1 to 45% depending on the series. In the American cen-ters, which have the greatest experience, the incidence isbetween 2.9 and 4.8% [24], although the actual incidence isdifficult to assess as occlusion of the GDA, LGA and RGA isoften at the discretion of the surgeons, as is investigating forpossible retroduodenal and supraduodenal arteries [25,26].

Despite the fact that occlusion of this artery is questionedby some authors [6], it remains recommended by the greatmajority of groups [2,3,10,21,27,28].

The presence and/or development of accessory RGAs(usually from the distal branches of the left branch of theHA) explain why some gastroduodenal ulcers develop despiteocclusion of the RGA [29]. 99Tc scintigraphy has a specificrole here, identifying gastrointestinal uptake and needs

to be examined carefully. Nevertheless, because ulcersdevelop as complications without uptake being seen ini-tially, it is not possible to restrict occlusion of this arteryto patients with extrahepatic uptake [30].

Figure 8. Technetium 99 scintigraphy after work up. Overlap-ping uptake onto the anterior aspect of the antropyloric region,suggesting extrahepatic diffusion of the spheres.

552 G. Vesselle et al.

Figure 9. Oblique MIP coronal CT reconstruction (a) showing the right gastric artery (arrow) and identifying a kink facilitating catheter-i

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zation during arteriography (b).

echnical tipsatheterization of the RGA is difficult because of its narrowiameter, occasionally tight proximal angle (Figs. 6 and 7)

nd many anatomical variants. Multiplanar CT reconstruct-ons are a valuable aid in some cases to identify its angleRAO, LAO) in order to define an appropriate view to workn, facilitating catheterization during arteriography (Fig. 9).

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igure 10. Selective catheterization of the left gastric artery (arrow)

rrow) (c) enabling it to be occluded proximally with coils (d).

icrocatheter (2.1/1.7 or 2.3/2.8 French)—microguides0.014 in) couples are usually required. The artery is thenccluded with 1.5 or 2 mm diameter coils. It is importanto ensure that its most proximal part is occluded because

f the presence of early dividing branches. Some authorsecommend extensive occlusion to reduce recruitment ofccessory branches [29].

(a and b) extending to the origin of the right gastric artery (double

Radioembolization with yttrium-90 microspheres work up 553

Figure 11. Opacification of the left branch of the hepatic artery (arrowhead) and a narrow right gastric artery (arrows) recognizableby its characteristic shape (a and b). As this could not be catheterized, a remodeling balloon was inflated at its ostium (arrowhead) (c).

reflu

Infusion of 90Y distally with a microcatheter (arrow) with no risk of

(double arrow).

As catheterization is difficult, it is essential that the guidecatheter is stable. Depending on the anatomical configu-ration of the celiac axis and the diameter of the MHA, aconventional catheter does not always provide sufficient

Figure 12. Oblique MIP CT reconstruction identifying the cysticartery (arrow) originating from the gastroduodenal artery (arrow-heads) and its two dividing branches (smaller arrows) (same patientas in Fig. 1b).

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x into the right gastric artery. Distal end of the balloon microguide

upport and advancing the catheter increases the risk ofeactive arterial spasm. In this case a more stable catheters highly recommended.

If direct catheterization is difficult, retrograde catheter-zation through the LGA is occasionally possible (in up to 89%f cases) [31] (Fig. 10). Because of the winding path of theGA and its length and fragility (particularly when it givesise to an aLHA), catheterization is difficult and occasionallympossible if plexiform anastomoses are present [21]. Simi-arly to the anterograde approach, it is important to reachhe ostium of the RGA in order not to miss some proximalranches.

If both anterograde and retrograde approaches fail,ne alternative is to achieve transient occlusion with

remodeling balloon. 90Y is then injected distally [18]Fig. 11).

One recent described technique may also facilitate occlu-ion of the artery when its particularly narrow diameteroes not allow a microcatheter to pass. This involves using

detachable hydrocoil as a microguide [32].

ractical considerations

ost authors recommend that this artery be occluded.

Several technical options are available to occlude it if itsnatomy does not allow conventional catheterization.

554 G. Vesselle et al.

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igure 13. Catheterization (a) and transient balloon occlusion of

ystic artery (CA)

he cystic artery is responsible for the main vasculariza-ion of the gallbladder and is the primary arterial supplyo the extrahepatic biliary tree [33]. It divides early intowo branches which run to the gallbladder, one superficialeritoneal branch and the second deep parietal branch. Itives rise to the right branch of the HA in 63.9% of people,he CHA (26.9%), the left branch of the HA (5.5%), the GDA2.6%), the superior pancreaticoduodenal arcade (0.3%) andhe SMA (0.8%) [34]. If it arises from the right branch of theA, its origin is often distal, close to the bifurcation betweenhe anterior segmental (segments V and VIII) and posterioregmental (segments VI and VII) branches. An accessory CAs present in 2 to 25% of people [34—36]. Secondary arte-ial supplies are common, arising mostly from perforating

ranches from the liver parenchyma and the GDA.

It is recognizable by its Y shape and can be identified onT and arteriography in most patients (Figs. 1b, 3a and 12).

igure 14. Falciform artery (arrows) originating from segment IVarrowhead).

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cystic artery (b) (same patient as Fig. 3).

Gallbladder complications due to diffusion of 90Y par-icles into the CA are rare, and the great majority ofatients do not develop any gallbladder complications.f they do occur, they mostly involve transient postpran-ial right hypochondrial pain, although up to 23% of casesre complicated by radiation-induced cholecystisis in someeries [37,38].

Several groups report that clinical symptoms resolve withedical treatment [37,38]. Prophylactic antibiotics withuroroquinolones was used routinely by some groups whenhe right lobe of the liver is being treated or more generallyhen clinical symptoms are present, although there is no

tatistical evidence that these are effective [39].It is not uncommon after RE treatment to see gallbladder

bnormalities on imaging, which appear as a thickening orven a defect of the gallbladder wall. These abnormalitiesre not specific and should not incorrectly suggest radiation-nduced cholecystitis, which is primarily a clinical diagnosis39,40].

The approach to the CA is controversial. Some authorsecommend that it be occluded whereas others believe thathe risk of ischemic cholecystitis is too great if it is.

The operator is then faced with several possible situa-ions and options. He/she should assess the risks of:

radiation-induced cholecystitis following proximal admin-istration to the CA;suboptimal diffusion of spheres in distal injection;ischemic cholecystitis if the artery is occluded.

Several types of CA occlusion are reported in the litera-ure, the most common of which are the use of Spongel coilsr inducing spasm with the microguide. Some authors pre-er temporary occlusion with Spongel [37,38]. The inducedpasms technique is less predictable, causing transientncomplete, unquantifiable stenosis and carrying a risk ofomplications (dissection or perforation) [37].

If gallbladder uptake is present, some authors are lessnclined to occlude a large diameter CA in order to reducehe risk of ischemic cholecystitis than when the diameter is

arrow, suggesting that collateral arterial supply constitutes

significant component (from the liver parenchyma or GDA)hich reduces this risk of ischemia [3,39]. As such, occlu-

ion of the CA carries less risk of ischemia when the GDA

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Radioembolization with yttrium-90 microspheres work up

is occluded very proximally, enabling gallbladder arterialsupply from its perforating branches [3,4].

Generally in the literature, most radiological gallbladderabnormalities are asymptomatic and very few cases haverequired surgery [37,39,40].

The existence of parasitic arterial supply to the tumorfrom the CA is a specific point which may result in hyper-selective occlusion of the branches of the CA to the tumorbefore injecting yttrium spheres [41] (Fig. 3d).

No cases of post-RE cholecystitis occurred in our seriesand the CA was seen on most of the arteriographies. Sig-nificant scintigraphy uptake was found in two patients:temporary occlusion with a remodeling balloon was per-formed in one case and the spheres were released distally inthe second case (Fig. 12). This type of temporary occlusionby a remodeling balloon is a transient solution which is safebut expensive and has been very little assessed/performedin published reports [18]. Only one permanent occlusion ofa CA arising from the proximal part of the GDA with coilswas considered necessary (Fig. 1b).

Practical considerationsWherever possible, preference should be given to low rateadministration of spheres distally in the CA.

If occlusion of the CA is necessary, very proximal occlu-sion of the GDA is recommended.

Occlusion with resorbable gelatin appears to be a sim-ple and effective method associated with few ischemiccomplications.

Temporary occlusion with a remodeling balloon is anattractive but not well assessed possibility (Fig. 13).

Radiological and clinical findings are often inconsistentand the clinical features should take priority in selectingany treatment options.

If cholecystectomy is being considered, this should bedeferred wherever possible to more than two weeks afteryttrium treatment in order to reduce irradiation to the oper-ator.

Falciform ligament artery

The falciform artery (FA) was described for the first time in1753 and originates from the distal branches of the LHA orMHA. It therefore usually arises from arteries supplying seg-ments IV (68%), III and the common trunk segments II andIII. Occasionally, it has been reported to arise from the rightbranch of the HA or the CA [20]. It runs in the falciform lig-ament alongside the para-umbilical vein and then spreadsout around the umbilicus and communicates with the dis-tal branches of the superior and inferior epigastric arteries[7,42].

It is recognizable by its ‘‘L’’ shape and craniocaudal pathalong the anterior abdominal wall. It is usually not seen onimaging (Fig. 14).

Anatomical series describe it in almost 70% of patientsbut it is only found in 10% of arteriography series, predom-inantly in prospective (25—50%) compared to retrospective

(2%) studies because of its distal origin and narrow diam-eter (0.7 mm) which requires a sufficiently high flow rateto be infused into the left branch of the HA, ideally in aRAO view, when it is better seen in the capillary and venous

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hases [43,44]. It is far more important and its diameter isncreased after laparotomy or stenosis/occlusion of the leftranch of the HA [44]. It is also better seen on selectiveepatic arteriography with helicoidal acquisitions [7].

Radioembolization complications due to spheres passingnto the FA are rare, mild and usually transient. The mostommon presentation is abdominal pain or an epigastric skinash which lasts from a few hours to a few weeks [45]. Theseenerally resolve spontaneously or with analgesia [43]. Aew cases of skin necrosis have, however, been describedollowing hepatic chemoembolization procedures [45—47].

The 99Tc scintigram must be examined carefully as anyptake in the abdominal wall due to spheres spreading intohe FA is usually low and may require multiplanar recons-ructions in a SPECT CT examination [48].

Although some authors recommend that this artery beooked for routinely and embolized prophylactically [3,45],he low incidence of complications and their usually mildature are such that other authors only do this if it is visiblen standard arteriography. This approach is very reasonables symptoms almost never develop even if uptake is seen oncintigraphy [43]. On the other hand, some groups recom-end that it be occluded if uptake is seen [3,49].The FA can be occluded by selective microcatheteriza-

ion and introducing microcoils (0.018). As it is less than aillimeter in diameter and arises distally, this procedure isifficult and occasionally unproductive [42,49].

ractical considerationshe consequences of diffusion of yttrium spheres into theA are rare and mild.

To find it, a specific angiography protocol is oftenequired.

Operators do not need to be concerned about this arteryf it is not seen on standard radiography or if no abdominalall uptake is seen on scintigraphy.

SPECT CT images should be read carefully and on multi-lanar reconstructions, as uptake from spheres passing intohe FA is low.

Knowledge of the existence of this artery and the pos-ible complications allow any painful abdominal symptomshich develop following the procedure to be recognized andnderstood.

etroduodenal, supraduodenal andetroportal arteries

he supraduodenal artery (SDA) supplies the horizontalortion of the first segment of the duodenum. It is reportedn almost 93% of surgical series [35] and has many varia-ions. It arises mostly from the GDA (27%), CHA and MHA20%) and from left (20%) and right (13%) of the HA [35,50].t is associated with similar complications to the RGA, whichs a reason for identifying and, where appropriate, occlud-ng it [3,9,27]. It may be responsible for parasitic arterialupply to the tumor [51]. Some authors describe occludinghe artery with biological glue [52].

The anterosuperior pancreaticoduodenal artery (ASPDA)formerly the retroduodenal artery) supplies the duodenalulb and the uncinate process of the pancreas. The origin ofhis artery also varies and is usually from the proximal part

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f the GDA but it may also arise from the CHA or MHA (15%)nd requires particular attention [50,53].

The retroportal artery arises from the proximal portionsf the CA (41%) or SMA (58%).

It contributes to the anastomotic arterial supply to thextrahepatic biliary tract [33,54] and communicates withhe posterosuperior pancreaticoduodenal artery (type I) orhe right branch of the HA (type II).

These arteries are rarely seen individually as they areecondary and of narrow diameter. When they are visiblend identified, however, embolization may be required [3].

When they are not easy to catheterize, temporary occlu-ion of the CHA with a remodeling balloon redistributes localemodynamics, reversing the flow in the GDA and thereforehe flow in these small arteries and avoiding adverse effectsue to particle introduction [18,55].

xtrahepatic arterial supplies to the tumor

he existence of extrahepatic arterial supply to neoplas-ic liver lesions and particularly hepatocellular carcinomaHCC) is well documented in the literature and affects 17o 30.8% of liver tumors [50,51,56—58]. These afferent sup-lies raise several problems. Failing to take account of suchn artery in RE by administering the spheres through theain hepatic pedicle carries a risk of only partial treat-ent, potentially missing the volume of tumor supplied by

hese branches and subsequently promoting future arte-ial changes to the benefit of these accessory branches.onversely, infusing 90Y through these branches, which areften narrow, requires occasionally difficult catheterization,natomical knowledge of potentially dangerous anasto-oses and fragmentation of the doses to be administered to

olumes of liver which are complicated to assess and atyp-cal. The injection must be administered at a low flow ratend appropriate to the diameter of the supplying artery.

Several factors predisposing to recruitment and develop-

ent of these branches have been identified. These include

previous history of chemoembolization, occlusion of theain arterial pedicle and also the size of tumor volume

63% of tumors over 6 cm), exophytic tumors, those located

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igure 15. Axial (a) and oblique coronal (b) reconstructions of an arlosely to a lesion in segment II (arrowhead).

G. Vesselle et al.

n the infracapsular area and contact with the area nuda50,56,58].

Three main options can then be considered:administering the spheres through these arteries;occluding them and therefore achieving a single hepaticpedicle;not considering them if their vascular supply appears tobe negligible.

Although many hepatic embolization and chemoem-olization procedures through these different arteries areeported in the literature (internal thoracic, phrenic,olonic and renal arteries, etc.) [51], few similar proceduresave been described for RE. Occlusion of these arteries canroduce a single hepatic pedicle by opening intrahepatichunts, restoring vascularization to territories which haveeen occluded by branches of the PHA. The viability of thesenastomoses for RE procedures has been demonstrated byeveral authors based on the arteriographic vascular changesfter arterial occlusion, the distribution of MAA uptake inretreatment scintigraphy and achieving tumor response inhese revascularized territories [58—61].

We will only describe the problems experienced when annferior phrenic artery is present, as the other arteries areignificantly less common.

nferior phrenic artery

he right and left inferior phrenic arteries (PA) arise usu-lly from the celiac axis and the abdominal aorta (40 and8% for the right PA respectively) although they also ariserom the renal arteries, the LGA and the CHA [62]. Theyay arise separately or through a common trunk, then divid-

ng into ascending and descending branches and may giveise to vascularizing branches, vascularizing the inferiorena cava, adrenal glands, inferior esophagus or give riseo accessory gastric and splenic branches. Communicationsith the internal thoracic, intercostal, muscular, phrenic

nd pericardial arterial systems are also seen and transpleu-al communications have been described, usually in patientsuffering from chronic lung diseases. Their phrenic anddrenal arterial supplies are constant findings [51,62].

terial phase abdominal CT. Right phrenic artery (arrows) running

Radioembolization with yttrium-90 microspheres work up 557

Figure 16. Opacification (a) then occlusion (b) of a large phrenic artery (arrow) in a patient with a large tumor mass in the dome of theatic a

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liver. Yttrium was then administered to the left branch of the heplobe of the liver, confirming spontaneous reopening of intrahepatic

The most common origin of the 17 to 30% of cases ofextrahepatic arterial supply to HCC tumors is the right PA(up to 50%) [41,50,51,56,57]. This proportion appears to beincreased if an aLHA is present [11] and after chemoem-bolization, as a result of arterial redistribution (up to 83%)[41]. A significant size of tumor contact with the diaphragmand being located in segment VII are factors in which thisartery is almost always involved [57]. Its involvement shouldalso be strongly suspected when the tumor blush is notpresent on arteriography. It is therefore a problem fre-quently encountered during RE procedures and this arteryshould therefore be identified routinely before treatment[2,3,35,63].

It is often increased in diameter when it is responsiblefor arterial supply to the tumor and can then be identifiedon a pretreatment CT [57,62] (Fig. 15). It can usually notbe seen on arteriography following a conventional injectioninto the celiac axis or MCA because its origin is extremelyproximal. It should therefore be looked for on aortography(right-sided or ‘‘pigtail’’ catheter) or by direct catheteriza-tion after identifying its origin on a section image (Fig. 16).

Its narrow diameter origin and path represent com-mon obstacles to catheterizing the artery, particularlywhen it arises from the proximal superior portion ofthe CA. ‘‘Shepherd stick’’ or ‘‘Simmons’’ cathetersare used most commonly and some people describeusing ‘‘homemade’’ catheters, equipped with a lateralorifice [64].

Some groups describe administering spheres through thePA after a detailed analysis of arterial supply as being bothachievable and useful and avoiding occlusion of the PA. Theconfigurations required to make this procedure safe are only,however, met in a small number of patients [51], and theidentification and occlusion of many anastomotic branchesrequired is sometimes complex and laborious.

Redirection of anterograde hepatic flow is an optiondescribed by Abdelmaksoud et al. [58]. This has been val-idated angiographically and scintigraphically and requires

distal occlusion of the PA, distal to its extrahepaticbranches, prior to administration of microspheres. Thisoption has the advantage of a conventional infusion ofspheres into the hepatic pedicle.

rofo

rtery after checking homogeneous technetium fixation in the leftts.

ractical pointshe PA is the most common extrahepatic arterial supply forCC.

In situ administration may cause various and potentiallyerious complications due to many extrahepatic afferentessels.

Opening of intrahepatic shunts as a result of occludinghe PA and administrating spheres through the main hepaticedicle is a more straightforward option and less likely toause extrahepatic complications.

ther extrahepatic arteries

he same applies to all of the other extrahepatic arter-es (omental, adrenal, intercostal, cystic, internal thoracic,enal, colonic and lumbar, etc.). Most of these are usuallyery narrow in diameter and for the most part have insignif-cant impact on the RE.

ignificant anatomic variants

ight hepatic artery (RHA)

epending on whether the embryonic hepatic arteries per-ist, several variants in the origin of the right branch of theepatic artery are seen. The most common is an RHA (ori-in of the SMA) (10 to 12% of cases) [20,65]. This artery canoexist with the right branch of the HA (it is then called anccessory RHA) or be the only artery in 3% of cases (replacedHA) [66]. Very rarely, the right branch of the HA arises fromhe pancreaticoduodenal arcades, the GDA (3.6%), CA (1.2%)r a phrenic artery [20,35,50].

It is important to identify these variants. This is doneasily on computer tomography images and involves lookingor an often proximal branch of the SMA running to the liver.

Two options are described in the literature, adminis-ration of spheres through the accessory RHA (aRHA) or

eplaced RHA (rRHA), or occluding the artery. The firstption requires calculating the distal hepatic volume andractionating doses, as the territory involved may includene or more liver segments. The arteriography—CT couple

558 G. Vesselle et al.

Figure 17. Catheterization of an accessory left hepatic artery (arrow) (a). Occlusion of the artery with coils and then removal of themicrocatheter (arrowhead) enabling opacification (b) then catheterization of the left gastric artery (double arrow). Contrast injection showsthe arcade of the lesser curvature extending to the origin of the right gastric artery (arrow) close to the origin of the already occludedgastroduodenal artery (c). Note the partial opacification of the main hepatic artery from which the right gastric artery arises (double arrow).The final check confirms retrograde opacification of the accessory left hepatic artery (arrowheads) and vascular distribution favoring thel

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eft branch of the hepatic artery (d).

hen plays a particular role, allowing a more detailed assess-ent of the territories. The second option, occlusion, isore straightforward and is based on the development of

ntrahepatic shunts. The territory to be recanalized is lessf an aRHA is present than if the RHA arises purely from theMA.

ractical pointsretreatment examination for a variant of the origin of theight branch of the HA should be performed routinely.

Administration of spheres through the main hepatic pedi-le after its distal occlusion is straightforward to performnd carries few complications.

eft hepatic artery (aLHA)

hese anatomical variants can similarly involve the leftranch of the hepatic artery. The most common is the

rigin of the left branch of the hepatic artery from theGA. This artery may be the only feeding artery of the leftepatic lobe (replaced LHA) or coexist with the left hepaticranch (accessory LHA). The prevalence of these arteries

tpth

ange from 3.8 to 10% and from 8 to 10.7% respectively [65]Fig. 17).

The left branch of the HA can also arise either as a singlertery or as an accessory from the GDA (1.2%) [20]. Whenresent, the small accessory LHA (aLHA) usually vascularizesegments II and III of the liver and, less frequently, segmentV [3]. These arteries should also be looked for.

These variants can usually be easily identified on the pre-reatment CT. The gastrohepatic trunk is usually seen in thessure of the venous ligament.

It may be possible to identify an aLHA or a replaced LHArLHA) indirectly by CT combined with arteriography whenncomplete left parenchymography indicates the existencef an external arterial supply.

This artery is fragile and readily spasms. Catheteriza-ion may be difficult and requires Simmons catheters [2,21]Fig. 18).

The existence of an aLHA or rLHA raises several problems,ost similar to those produced by variants of the origin of

he right branch of the HA. Identification of possible extrahe-atic branches is an additional difficulty. Branches supplyinghe diaphragm, esophagus or stomach carry a risk of extra-epatic complications when spheres are infused through

Radioembolization with yttrium-90 microspheres work up 559

Figure 18. Another patient with an accessory left hepatic artery (arrow). Left gastric artery (small arrows) (a). Attempted catheterizationof the accessory left hepatic artery complicated by dissection of the left gastric artery at its origin (b). Insertion of two stents (arrow)recanalizing this artery (double arrow) and occluding the accessory left hepatic artery (arrow) (c). Note the presence of embolic material

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ac

c

O

Mdence of a double hepatic artery, hepatic arteries arisingdirectly from the CA or the aorta, and a GDA arising

in the right gastric artery (coils) and gastroduodenal artery (plug).

this artery [2,3,11,35]. If a rLHA is present, these variousbranches should be embolized [2]. They are often narrowand winding, usually arising from the proximal horizontalportion of the aLHA and making the procedure occasionallydifficult, particularly as catheterizing the LGA may be com-plicated and unstable. An indirect sign of the presence ofthese extrahepatic branches is the opacification of a left gas-tric vein, providing venous return from part of the stomachand inferior esophagus.

In exactly the same way, the option of occluding andinfusing spheres through the main hepatic pedicle wouldappear more straightforward and carry less risk of extra-hepatic complications.

Some authors have maximized this approach by creat-ing a single hepatic pedicle going as far as occluding anhepatic artery (usually the left branch) and administeringthe spheres through the right branch of the HA with homo-geneous distribution of uptake throughout the whole liver[59—61]. This option would appear to simplify all the proce-dures.

Tips and tricksIt is essential to look for an accessory or a replaced LHA.

This is seen easily in the fissure of the venous ligament whenpresent.

It must be catheterized cautiously as the trunk readilyspasms.

f(ta

Spheres may be administered through this artery but car-ies risks of complications due to the presence of branchesupplying extrahepatic tissue, which should be identifiednd occluded first.

Occluding these arteries redistributes the intrahep-tic arterial flow by opening anastomoses and creating

single hepatic pedicle and allows the spheres to bedministered through the main hepatic pedicle. Thisption has been successfully confirmed in several studies59—61].

Retrograde opacification of this artery or reestablishing complete hepatic parenchymography on the final reviewonfirms the intrahepatic arterial redistribution.

It is recommended that a Simmons catheter is used foratheterization for better stability.

ther variants involving the main arteries

any other variants of the origin of the HA and RHA areescribed in the literature, the main ones being the pres-

rom the aorta or the SMA. These variants are very rare<2%) [20,65], and are usually recognizable on the pre-reatment scan. They do not require any specific technicalpproach.

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onclusion

he preparatory phase for hepatic radioembolization pro-edures is a key stage and relies on good knowledge of theepatic vascular anatomy and its subtleties.

isclosure of interest

he authors declare that they have no conflicts of interestoncerning this article.

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